Sameness in Biology

Sameness in BiologyAuthor(s): Grant Ramsey and Anne Siebels PetersonReviewed work(s):Source: Philosophy of Science, Vol. 79, No. 2 (April 2012), pp. 255-275Published by: The University of Chicago Press on behalf of the Philosophy of Science AssociationStable URL: http://www.jstor.org/stable/10.1086/664744 .Accessed: 26/03/2012 10:40

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Philosophy of Science, 79 (April 2012) pp. 255–275. 0031-8248/2012/7902-0004$10.00Copyright 2012 by the Philosophy of Science Association. All rights reserved.

255

Sameness in Biology*

Grant Ramsey and Anne Siebels Peterson†‡

Homology is a biological sameness relation that is purported to hold in the face ofchanges in form, composition, and function. In spite of the centrality and importanceof homology, there is no consensus on how we should understand this concept. Thetwo leading views of homology, the genealogical and developmental accounts, havesignificant shortcomings. We propose a new account, the hierarchical-dependency ac-count of homology, which avoids these shortcomings. Furthermore, our account pro-vides for continuity between special, general, and serial homology.

1. Introduction. It is indisputable that many distinct biological entitiesbear the relation of “sameness” to one another but less clear what factsdetermine this sameness. One reason for this is that sameness is not ahomogeneous category: there is sameness of function, of form, or ofcomposition. Two proteins, for example, may consist of identical stringsof amino acids, making them compositionally the same (possessing thesame “primary structure” in the parlance of the biologist), but they maybe folded differently, making them different in form (different in theirsecondary or higher structure). And this difference in form may bringabout a functional difference, changing the role that the protein plays inthe physiology of the organism. These three kinds of sameness are inter-esting and in want of philosophical scrutiny, but the focus of this articlewill be a fourth kind of sameness, one much more mysterious. This kind

*Received April 2011; revised August 2011.

†To contact the authors, please write to: Grant Ramsey, Department of Philosophy,100 Malloy Hall, University of Notre Dame, Notre Dame, IN 46556; e-mail: [email protected]; Anne Siebels Peterson, Department of Philosophy, 100 Malloy Hall,University of Notre Dame, Notre Dame, IN 46556; e-mail: [email protected].

‡We thank Marc Ereshefsky, Russell Powell, Phil Sloan, Gunter Wagner, two anon-ymous reviewers, and the editor of this journal for their helpful comments on thisarticle. Some of the ideas for this article were presented at the 2011 meeting of theInternational Society for the History, Philosophy, and Social Studies of Biology. Wethank the audience members for their thoughtful suggestions.

mailto:[email protected]



256 GRANT RAMSEY AND ANNE SIEBELS PETERSON

of sameness, known as “homology” by biologists, is mysterious becauseaccording to it the sameness relation is purported to hold in the face ofchanges in composition, form, and function. The great anatomist RichardOwen, who coined the term, defined a homologue as “the same organ indifferent animals under every variety of form and function” (1843, 379).

Before Darwin, we had at least one clear answer to the question ofwhat facts fixed sameness in the homological sense: a fundamental divineblueprint or “archetype” that, like a Platonic form, is eternal and un-changing. Owen astutely determined that it is not just that similar spe-cies—kudus and zebus, say—exhibit the same parts (tails, legs, ribs, etc.)but that almost every individual trait (each bone, say) in each of thesespecies has a corresponding part in a wide range of taxa. For Owen, whatmade these organs instances of the same thing was not their similarity(since many homologues are quite dissimilar) but their correspondence tothe same features of the vertebrate archetype.1

With Darwin came the downfall of the eternal, fixed archetype in bi-ology. Instead of viewing species as having fixed essences, Darwin un-derstood them as collections of individuals that vary from one anotherand that evolve over time, adapting to local circumstances. One mightsuppose that homology would also have met its end at the hands ofDarwin, that the concept would have been discarded along with Owen’sarchetypes. But not only did Darwinism not annihilate homologies, itturns out that homologies are at its very basis. In order to make a claimthat a trait has evolved (e.g., that jaw structure has changed), the sametrait must be picked out in different individuals (the jaw in organisms A,B, C, etc.). Darwinism thus undermined the traditional basis for homologyonly by making key use of the notion of homology. In the wake of Darwin,then, biologists and philosophers had to ask whether there is a new foun-dation for homology.

The idea that homology is at the core of biology has persisted to thisday. In the words of contemporary biologist David Wake, “Homology isthe central concept for all of biology. Whenever we say that a mammalianhormone is the ‘same’ hormone as a fish hormone, that a human genesequence is the ‘same’ as a sequence in a chimp or a mouse, that a HOXgene is the ‘same’ in a mouse, a fruit fly, a frog, and a human . . . wehave made a bold and direct statement about homology” (1994, 268). IfWake is right, then having a clear sense of the nature of homology is of

1. Owen understood the archetype both as an ideal form and as an immanent dynamiclaw. The archetype thus answered two questions: what facts make a trait in one or-ganism the same as that in another? and, what explains the pattern of form acrossdiverse taxa? We are here focused on the answer to the first question. See Sloan (2003)for a discussion of this dual nature of the archetype.

SAMENESS IN BIOLOGY 257

central importance for understanding the conceptual foundations of bi-ology.

Although some are skeptical that a single, unifying concept of homologyis achievable (Griffiths 2007), we disagree. In what follows, we argue thatpast attempts to provide an archetype-free foundation for homology havefailed. But we do not take this as a call for the abandonment of homologyor the reintroduction of the archetype. Instead, we propose and defenda novel way of understanding homology. Our proposal retains the originalsense of homology as biological sameness while doing away with arche-types. To motivate our account of homology, we will first show why theconcept of sameness must be at the core of homology and then why theother leading attempts to ground the concept of homology have failed.

2. Sameness, Not Similarity. The problem of homology determination isthe problem of taking traits that vary and classifying them as the same.This classification task would not be necessary if homology were basedon similarity instead of sameness. For this reason, it is tempting to con-sider homologies to be based merely on similarity. Some authors havedone just this, for example, “homology is resemblance caused by a con-tinuity of information” (Van Valen 1982, 305), while others move backand forth between sameness and similarity without sharply distinguishingbetween them or asserting that only one should be linked to homology.For example, Neander and Rosenberg (2009) say of homologues that“their sameness or similarity can be explained by their common descent”(309, emphasis added). Similarly, Hall (2003) defines homology as “sim-ilarity because of common descent and ancestry” (409, emphasis added)in one place and as “the same character continuously present in two taxaand in their most recent common ancestor” (419, emphasis added) inanother place within the same article.

Unlike these authors, we feel that one should sharply distinguish same-ness from similarity because homology needs to be based on sameness,not similarity.2 There are three reasons for basing homology on sameness.First, although many traits identified as homologies are in fact similar,this is not always the case: my femur and the femur of a chicken aresimilar, but the malleus bone in the mammalian inner ear is not similar(in form, position, or function) to the articular bone in a reptile since thelatter is part of the jaw and the former is a small hammer-shaped bone

2. Others have emphasized homology as sameness; e.g., Ghiselin suggested that “muchof the confusion about homology has resulted from treating correspondence as if itwere similarity” (2005, 92).


attached to the eardrum.3 A second reason for basing homologies onsameness instead of similarity is that sameness, but not similarity, is tran-sitive. If trait T1 is similar to T2 and T2 is similar to T3, it does notfollow that T1 is similar to T3. It is for this reason that one who defineshomology merely in terms of similarity cannot classify cryptic homologies(like the malleus and articular bones) as homologies.

For the third reason for basing homology on sameness, consider thedefinition of homology by Hall (2003) quoted above, “similarity becauseof common descent and ancestry,” which is typical of how homology assimilarity is defined. How are we to read “because of” in this quote? Wecould read it definitionally or causally. If we read it definitionally, then itmeans that we are defining something as “similar” just in case it is sharedthrough descent and ancestry. There are two problems with this reading.First, this is a violation of what we mean by “similarity”—we do not takecommon ancestry to be a necessary or sufficient condition for similarity.Second, it smuggles sameness into the definition, for what are claims ofcommon descent and ancestry if not claims about common ancestorspossessing the same trait? In other words, although this account of ho-mology is prima facie based on similarity, it presupposes an appeal tosameness.

If we instead read the “because” in “similarity because of commondescent and ancestry” causally, then the statement is too strong. Underthis reading, the claim that trait T is homologous in taxa X and Y impliesthe truth of this counterfactual: had the ancestor of X and Y not had T,then X and Y would not have T. Thus, the claim that velvet worm eyesand arthropod eyes are homologous would be true only if it is the casethat had the ancestor of the Onychophora and the Arthropoda not hadeyes, the Onychophora and the Arthropoda would not have eyes. But thisis too strong, since it is conceivable that the Onychophora and the Ar-thropoda could have separately evolved eyes had their common ancestorlacked eyes.

Weaker ways of understanding causation in this context could be for-mulated—for example, causation might be understood probabilistically.The fact that the ancestor of X and Y possessed T might merely raise theprobability of X and Y possessing T. Thus, the claim that velvet wormeyes and arthropod eyes are homologous would be true only if it is thecase that their independent evolution would have had a low probability.But such a reading of this causal claim would not help the situation. Forthe probabilities of evolving eyes in these lineages are independent of

3. There are some similarities in this case, of course, like similarity of composition(both are made of bone), but there is nothing preventing composition or other featuresfrom changing over time while homologousness is retained.


whether Onychophora and Arthropoda eyes are homologous: even if theprobability of evolving eyes independently were 0.99, this would notchange the fact that they are homologous. (Analogously, the fact thatsomeone was killed by a bullet is not undermined if it turns out that theyhad a 0.99 probability of dying of a heart attack had the bullet not donethem in.) Moreover, employing the probabilistic understanding of cau-sation in reading this claim would, if anything, only make it more difficultto test claims of homologousness.

In addition to these conceptual difficulties with this causal reading of“because of,” it also goes against actual biological practice and would beoverly burdensome for biologists were it imposed. Not only would bi-ologists need to prove common ancestry of a potential homologue, butthey would have to show that had the ancestor lacked the trait, it wouldnot have appeared—or would probably not have appeared—in the de-scendants. If this burden of proof were levied on biologists, claims ofhomologies would all but cease.

We are led, therefore, to conclude that homologies must, in the spiritof Owen, rest on a foundation of sameness. The challenge, then, is toaccomplish this without invoking eternal, static archetypes. There havebeen two main attempts to accomplish this, and each, we will see in thefollowing section, falls short of the goal.

3. In Need of a Theory. Founding homologies on sameness instead ofsimilarity gets us out of the difficulties just elaborated. But there is a cost.Similarity is, in some sense, more basic, more prior to, and independentof theory. Sameness, on the other hand, requires theory to be able todigitize the continuous variation in the world into “same” and “not same.”How is this digitization to be accomplished? Before proffering our answer,we will consider how others have answered.

The two most prominent accounts of homology are the genealogicalaccount and the developmental account.4 According to the former, generallyput, traits in different organisms count as homologous if and only if theorganisms in which each is found share a common ancestor with the sametrait. It is this account that we employed in section 2 in our discussionof the meaning of “because of” in accounts of homology that considertraits to be homologous “because of” their existence in shared ancestors.The central difficulty with the genealogical account, as we have just seen,is that it seems to beg the question. It purports to give us criteria for the

4. The genealogical account, also called the evolutionary account or taxic account ofhomologies, is the view of homology advanced by Darwin (1859) and elaborated andmodified by others, e.g., Patterson (1982) and de Pinna (1991). The developmentalaccount is classically explicated by Wagner (1989).


homologousness (i.e., sameness) of traits in different organisms but helpsitself to the notion of what it would be for a trait in a common ancestorof these organisms to be the same as the traits in each of the organisms.As Wagner (1989) points out, since traits pass on their structure onlyindirectly, through the reproduction of the organisms in which they arefound, the ancestral trait/descendent trait relation is not manifest andunproblematic in the way that the ancestral organism/descendent organismrelation is. Hence, it cannot be taken for granted. But if we had an answerto the question of what makes the trait the same in the ancestor and thedescendants, this would also serve as an answer to the question of whatit would be for the traits of the two original organisms to be homologous.The genealogical account thus analyzes homology between two traits onlyby taking for granted homology between each of these traits and a traitin an ancestral organism (Brigandt 2002).

Furthermore, if shared ancestors with the same trait are required forhomologies, then traits cannot be homologous between ancestor-descen-dent pairs. But this would be too exclusive. Given two organisms, X andY, there are three ancestor-descendent relationships that they can bear:X can be an ancestor of Y, Y can be an ancestor of X, or X and Y canshare a common ancestor without one of them being the ancestor of theother. In the scenario where X is the ancestor of Y, it could be that thetrait in question, T, arose in X for the first time. Thus, X and Y shareno common ancestor with T, yet it would be a mistake to conclude thatT is therefore not homologous in X and Y. These and other difficultieswith the genealogical account have compelled some to seek an accountof homology based on development instead of genealogy.5

In contrast to the genealogical account, the strategy of the develop-mental account is to count two traits as homologous if and only if theyare products of the same developmental phenomenon. More specifically,Wagner writes, “Structures from two individuals or from the same indi-vidual are homologous if they share a set of developmental constraints,caused by locally acting self-regulatory mechanisms of organ differenti-ation” (1989, 62). This account is not circular, but it faces difficulties justas grave as those faced by the genealogical account. First, on the practicalside, its adoption would severely undermine the practice of paleontology(not to mention other areas, like comparative anatomy). The paleontol-ogist does not require additional evidence about the development of aparticular bone over geological time in order to support a claim of ho-

5. For those wishing to bite the bullet and maintain that homologies require commonancestory, we would point out that a notion of sameness is needed to identify the traitin question in the ancestor as the same as those in the descendents. And if one needsthis notion of sameness, why not include it under the rubric of homology?


mology—indeed, such evidence is for the most part absent. If the devel-opmental account were adopted, paleontologists would, for every putativecase of homology, have to discern whether the developmental basis fortwo traits had persisted over time. Furthermore, it has long been rec-ognized that the developmental basis for a trait can change over time.Owen (1848) asserted this when he argued that “there exists doubtless aclose general resemblance in the mode of development of homologousparts; but this is subject to modification, like the forms, proportions,functions and very substance of such parts, without their essential ho-mological relationships being thereby obliterated” (6). While paleontol-ogists have departed from archetypes, they have not, for good reason,moved to developmental constraints as the basis of homology.

In addition to this practical difficulty, though, the developmental ac-count suffers from an even more fundamental problem: it gives us anaccount of homology for traits that are the product of development onlyby presupposing a distinct account of homology for developmental con-straints. This would not be unsatisfying were the account to appeal tohomology at the genic level instead, for, as Brigandt (2002) argues, ho-mology at the genic level is relatively unproblematic (genes reproducefrom ancestral gene templates and thus sameness of genes is based inwhether the genes are made from the same template). But the same is notthe case for the level of developmental constraints. And pretty clearly, thehomology of developmental constraints cannot simply be taken to super-vene on the homology found at the genic level, for it could be the casethat homologous developmental phenomena are underlain by differentgene sequences (e.g., this might happen over time within a single lineage).So, the developmental account presupposes a further substantive accountof the homology of developmental constraints. But for all we know, thequestion of what makes these developmental constraints homologous isjust as difficult to answer as the question of what makes the products ofdevelopment homologous, and if so, the developmental account onlypushes the brunt of the problem back a step.

We will now argue that there is an account of homology that avoidsthese difficulties. Ours is a hybrid account, drawing on the strengths ofboth the developmental and genealogical positions while avoiding theirshortcomings.6

4. The Hierarchical-Dependency Account of Homologies. We have shownthat both the genealogical and developmental accounts suffer from deep

6. Other hybrid accounts have been suggested (e.g., Abouheif 1997; Laubichler 2000;Wagner 2007; Ereshefsky 2009), although none of these accounts has suggested com-bining development and genealogy in the way that we propose to do so in sec. 4.


problems. We will now introduce a novel account of homology that at-tempts to evade these problems as well as to capture the right set ofphenomena and thus accord with and ground scientific practice.

Our account is based on hierarchical levels, and thus before we intro-duce our account, we must say a few words about these levels. Althoughthe account requires that there be distinct, independently individuatablelevels in organisms, it has no stake in the nature and quantity of the levels.Keeping this flexibility in mind, in what follows we will assume for thesake of exposition that there are just three levels. These levels, from bottomto top, are L1 (the genes employed by the developmental module), L2(the developmental module(s) responsible for the product), and L3 (theproduct of development such as a morphological or behavioral trait). Wewill use “L” generically to refer to one of the levels, “L-1” to refer to thenext level below L, and “L-2” to refer to the level below L-1. We ac-knowledge that an argument could be made, for example, that there is a“gene network” level between the gene and developmental module levelsor that there is a behavioral level above the morphological level. Thismore complex layering would not challenge our account of homology—our account merely requires the existence of levels.

We can now introduce our account, which we will label the hierarchical-dependency account of homology:

Homology.—Traits T and T* at level L belonging to organisms Oand O*, respectively, are homologous just in case:

1. There is complete continuity: Each organism in the shortest path(on a phylogenetic tree) traveling from O to O* possesses T, andeach from O* to O possesses T*. In the absence of completecontinuity of T/T* at L, the gap can be bridged if the features ofthe organism (from which T/T* is derived) at L-1 are continuouslypresent over the gap.

2. There is correspondence: In each organism along the path, T andT* must be numerically identical. (If there is complete continuityfrom O to O* without T and T* being numerically identical inevery organism along this path, then if T and T* are derived froma single feature at the next level down either in O and O* them-selves or in an organism ancestral to both O and O*, T and T*are homologous at a higher level of generality—they are what welabel g-homologous.)

In order to best understand this conception of homology, consider figure1. This figure has phylogenetic trees with ancestor Z and descendants Xand Y. The three lines represent continuity in the presence of a morpho-logical or behavioral trait (top line) and in the underlying developmental


Figure 1.

(middle line) and genetic (bottom line) material responsible for bringingabout this trait. In figures 1a and 1b, the trait at L3 is homologous betweenX and Y, since there is continuity at L2. However, in figure 1c, the trait atL3 is not homologous between X and Y because of a lack of continuity atL2.

This is not to say that the hierarchical-dependency account of homol-ogies (HDAH) has solved all of the problems of homology. One bigquestion lurking in the background is the following: What is the properway to individuate traits? Our account assumes that (1) the traits at eachlevel can be individuated, (2) the individuation of one level is separablefrom the individuation of another (e.g., the developmental level is notmerely individuated based on products of development), and (3) traitsbear quantifiable similarity relations to one another (see sec. 4.3 for whythis is the case). Although the full implementation of the HDAH requiresitems 1–3, this is true of the other accounts of homology as well. Ourproposed account of homology needs further explication, clarification,and justification, the task to which we now turn.

4.1. No Further Account of Homology Presupposed. The developmen-tal account of homology at L3 falters because it presupposes a prioraccount of the homology at L2, without giving an account of homologyat this level. Our account makes no such presupposition, for T and T*can refer to an entity at any of the three levels; hence, our account doesnot presuppose, but instead explains, lower-level homologies. If T and T*refer to something at the product of development level, then any gap inthe shortest phylogenetic pathway between them can be bridged if thereis continuity at the level of the developmental module responsible for thetrait’s production (as depicted in the path from X to Y in figs. 1a and1b). If T and T* refer to something at the level of the developmentalmodule, any gap in the shortest phylogenetic pathway between them can


be bridged if there is continuity at the level of the genes employed by thedevelopmental module. However, once we reach the genic level, completecontinuity on the shortest phylogenetic pathway from O to O* is a nec-essary condition for the homology of T and T* since there is no lowerlevel of continuity that can be appealed to as a principle for bridging agap in this pathway. But this result is not counterintuitive; if there is nocontinuity at any level, there is no reason to consider the traits on eitherside of the gap to be homologous. Therefore, our account applies tohomologues at every level; at no level does the account presuppose somefurther (unexplained) account of homology in the way that the devel-opmental account does (as pointed out in sec. 3).

4.2. Epistemological Worries. Our account of homology implies analgorithm for determining whether two traits are homologous: first, in-vestigate the continuity and correspondence of the trait. If it meets bothof these conditions at L, it is homologous. If it fails to be continuous atL, investigate whether there is continuity and correspondence at L-1 overthe gap in L. One may be tempted to object to our account because thisalgorithm will not be executable in practice for any interesting cases ofhomology. Even if there were fossils of all the individuals from O to O*,information about the basis of T/T* at L-1 would be all but impossibleto access, since it is not likely to fossilize. If our account did indeed requiresuch information to tell whether two traits were homologues, it would bea failure in this respect. But fortunately such a process is not necessaryfor determinations of homology. The algorithm shows what informationwould be needed to make diagnoses of homologousness in all situationsand with complete certainty. In practice, one will often use indirect in-formation to investigate possible homologies. For example, features ofmorphological traits (especially nonadaptive features unlikely to be pre-sent in convergences) may support the idea that these traits were producedby the same developmental module(s) without the presence of direct evi-dence for continuity at the developmental level. Indeed, a similar methodis employed for many other concepts in science. For example, the tem-perature of gas is understood as the mean kinetic energy of the moleculescomposing the gas. The algorithm implied by this definition for deter-mining the temperature of a volume of gas would be to record the mo-menta of all of the molecules in the volume, sum these values, and thendivide by the number of molecules. The fact that such an algorithm couldnever be executed in no way undermines the account of temperature ormakes it impossible to tell what something’s temperature is. Instead, thereare many indirect ways of determining the mean kinetic energy, such asby observing the expansion of mercury in a tube or the deflection of abimetallic strip. Moreover, on our account such indirect ways of deter-


mining whether there is continuity at the developmental level would onlybe needed in cases in which there is a gap in continuity at the level ofthe trait. On the other hand, as previously pointed out, given the devel-opmental account of homology, such indirect tests would have to be per-formed in every case.

4.3. Sameness from Similarity. Continuity requires sameness, butwhence does sameness derive in the absence of a typological account ofhomologies? If organisms were built by template matching—that is, ifeach organism were formed directly from an adult organism’s pheno-type—then sameness would merely consist in template-copy correspon-dences: T* in an offspring would be the same as T in the parent just incase T* was formed from the T part of the parental template. As it turnsout, however, things are much more complex. Organisms are rebuilt ineach generation, making correspondences more difficult to discern andrequiring sameness to be inferred from similarity. We have argued insection 2 that homologies consist in sameness, not similarity. Althoughthis is true, similarity is needed for sameness in the following way: whenmoving between O and O*, the sameness of the traits from one generationto the next is derived from their similarity (in form, but also in the “relativeposition and connection of the parts”; Owen 1848, 6). Although the mal-leus bone in the mammalian inner ear is not similar to the articular bonein a reptile, the bone in each parent-offspring pair (in all likelihood)exhibited similarity. It is this similarity in parent-offspring pairs that allowsus to conclude, at each step of the way, that we are still referring to thesame trait. If there were not similarity at the level of the bones, then therewould be similarity at the developmental level. And if there were nosimilarity at any level, the trait in question should be considered an evo-lutionary novelty, and T/T* should not be considered a homologous pair.

Because we build our account on the foundation of similarity, it mightseem tempting to infer that there is no reason to bring sameness into theaccount. But a key reason, as mentioned above, is that transitivity isrequired for homologies that span more than one generation (as all in-teresting ones do), and sameness, not similarity, exhibits transitivity.

4.4. The Nature of the Hierarchy and the Reason for Dependency. Hall(2003) incisively noted that homology can occur at multiple levels andthat there is a degree of independence between these levels—homologyat one level does not imply homology at other levels. A morphologicaltrait, say, could be homologous without the underlying genes or devel-opmental module(s) exhibiting homology. We agree. But, as our accountmakes clear, we are arguing for a certain kind of dependency between thelevels. The reason for this dependency is that, without it, many traits that


seem clearly homologous (and are identified by biologists as such) wouldnot be classified as homologous. Consider the unique dominance displaysperformed by alpha males in a number of species. If we were to take twoalpha males in one of these species and ask whether their dominancedisplays are homologous, operating under a strict rule of continuity, wewould likely infer that the behaviors were not homologous. The reasonis that there is a good chance that some of the ancestors (including themost recent common ancestor) were not alpha males (since although thealpha males often do the bulk of the breeding, they do not do all of it).We thus need the appeal to interlevel dependency in our account in orderto identify the behavior of the alpha males as homologous.

Although this is a within-species example, homology comparisons aretypically cross-taxa comparisons. One could simply extend this exampleto such a case. Let us say that a new species of chimpanzee is formedfrom Pan troglodytes. If we investigate the alpha male dominance displayand note that the new clade was formed by a non–alpha male (thus lackingsuch behaviors), it would be wrong to therefore conclude that the behavioris not homologous in the two species. The social Hymenoptera provideanother example. It makes sense to ask whether the fungiculture behaviorsshared by attine worker ants are homologous even though all such antsare infertile (and thus have neither progeny nor ancestors with the trait).A strict genealogical account—such as Hall’s “the same character contin-uously present in two taxa and in their most recent common ancestor” (2003,419, emphasis added)—would incorrectly rule out such cases as potentialhomologues if one interprets “continuously present” to operate at the levelof individuals (as parent-offspring continuity). If one instead interprets“continuously present” at a higher level (present in the population or presentin the species), then the above cases do not serve as counterexamples, buthomology so defined would be too permissive: consider a trait that existsin one part of the species, separately evolves in another part, and then goesextinct in the first part. The trait is thus continuously present, but the pastand present versions are not homologous.

One advantage of our account is that traits can be homologous evenif there is a gap at the level of the trait, L, as long as there is no gap atL-1, and this gap can occur anywhere along the path from O to O*, evenin the most recent common ancestors (as in fig. 1b). This is an advantage,since in cases like the social Hymenoptera or alpha males, it is clear thatthe continuous presence of a trait is too strong a criterion for homology.It is also true that homologies are not equivalent to shared, derived traits,that is, synapomorphies (pace Patterson 1982; de Pinna 1991). A trait canbe homologous between members of a clade without being shared—with-out, that is, all of the members of the clade possessing the trait. And atrait can be homologous without being derived (i.e., absent in ancestors).


Figure 2.

Thus, neither being derived nor being shared is a necessary condition forhomologies.

5. Distinguishing Homologies, Homoplasies, Homocracies, and Deep Homol-ogies. Homoplasy is contrasted with homology, and the two are oftenthought to be opposites. For example, Hall writes, “Homology is simi-larity because of common descent and ancestry, homoplasy is similarityarrived at via independent evolution” (2003, 1). But because our accountdoes not define homologies in terms of similarities, we have broken thesymmetry of this relationship. Under our account, homologies includeboth similar and dissimilar traits, while homoplasies include only similartraits (fig. 2). How does our framework categorize convergences, paral-lelisms, reversals, rudiments, vestiges, and atavisms?

Like the account of Hall (2003), our framework classifies convergenceas the only class of traits that is clearly homoplastic—convergences aresimilarities that are not homologous and thus fall in the striped portionof figure 2. Rudiments and vestiges are clearly homologous under ouraccount, since these are traits exhibited by ancestors and still present,although in a diminished/modified form, in extant individuals. Reversals/atavisms are traits not present in recent ancestors, but they are presentin both distant ancestors and current forms.7 The HDAH frameworkcategorizes such cases as homologies just in case the trait(s) at the next

7. The distinction between atavisms and reversals is usually made in terms of frequencyof occurrence—atavisms occur in few of the current forms, while reversals occur inmost or all of the current forms. See table 1 in Hall (2003).


level down (on which it depends) exhibits continuity and correspondenceover the span in which the trait is absent.

The implications of the HDAH for parallelisms will be more contro-versial than for these other categories, since parallelisms are often cate-gorized as homoplasies, not homologies. Recall that under our account,a trait at level L is homologous if there is continuity and correspondenceat L or, if there is not complete correspondence at L, if there is continuityand correspondence at L-1. Because the HDAH makes no restrictionsregarding whether this gap occurs during a branching event or in theabsence of branching, level L parallelisms are properly considered to behomologous as long as there is continuity and correspondence at L-1. Acase of homologous parallelism is represented by figure 1b.

Although our view accords in some ways with Hall (2003), there aresome important differences. Hall sees a continuum “extending from ho-mology r reversals r rudiments r vestiges r atavisms r parallelism”(412). Our view does not take this to be a continuum. Instead, the HDAHdistinguishes cases of gapless evolution (rudiments and vestiges) fromgappy evolution (reversals, atavisms, and parallelism). There may be con-tinua within each of these categories (e.g., gap size can vary continuously),but each of these categories does not occupy a spot in a larger continuum.

While convergences, as just shown, are categorized by the HDAH ashomoplasies, in many cases of convergent evolution the traits have beenbuilt in part from the same genes. Take the well-known case of PAX6,for example. Not only does the PAX6 gene have something to do witheyes in such disparate taxa as insects and vertebrates, but some mutationsin the gene will produce similar effects across these taxa, like aniridia inhumans, Small eye in mice, and ey in Drosophila (Quiring 1994). This issurprising, since the most recent common ancestor of these taxa lackedeyes, or at least anything resembling the eyes in these extant taxa. Thesimilar way in which the same genes are being employed in eyes and otherfeatures of distantly related taxa has compelled some to refer to thesetraits as exhibiting “deep homology” (Shubin, Tabin, and Carroll 1997).The HDAH framework correctly places deep homologies outside of thecategory of homology proper—deep homologies are not a kind of ho-mology but fall under a related concept. A deep homology is a trait thatis in part built from homologous genes (or gene networks). In deep ho-mologies, there is not continuity at either L3 or L2 but only at L1 (seefig. 1c), and continuity at L1 does not suffice for homology at L3. Nielsenand Martinez (2003) recognized this and introduced the term homocracyfor “organs/structures which are organised through the expression of iden-tical patterning genes” (149) to help stem the homocracy-homology con-flation. Because homocracies can (and often will) underlie homologies,


homocracy is a broader category than deep homology: deep homologiescan be understood as nonhomologous homocracies (see fig. 2).

6. Homology at Higher Levels of Generality. Our account of homologyhas the benefit of accounting for both homology in the strictest sense andhomology at a higher level of generality (hereafter g-homology).8 Fur-thermore, as we will see below, on our account g-homologies are the basisfor another type of homology, serial homology, which is often taken tobe quite distinct. (Serial homology is the relationship of homology fortraits within an organism—e.g., multiple vertebrae in the spinal column.)Our account is thus unifying, bringing serial and general homology underthe same rubric. Let us now draw out the implications of g-homologyand show how it is related to serial homology.

6.1. Levels of Generality. Just as the first condition in our account ofhomology (the continuity condition) asserts that there are distinct hier-archical levels at which homology can be exhibited, the second conditionnotes that there are multiple levels of generality at which homology canbe exhibited. Support for such a notion of homology at higher levels ofgenerality can be found in, for example, Shubin et al. (1997): “Deter-mination of whether two structures are homologous depends on the hi-erarchical level at which they are compared. For example, bird wings andbat wings are analogous as wings, having evolved independently for flightin each lineage. However, at a deeper hierarchical level that includes alltetrapods, they are homologous as forelimbs, being derived from a cor-responding appendage of a common ancestor” (647). Some authors whohave noted that homology can occur at multiple levels of the hierarchyhave not sharply distinguished hierarchy from generality. Hall, for ex-ample, asserts that “both homology and homoplasy can be defined atdifferent levels without making judgments about homology or homoplasy,or lack of homology/homoplasy at other levels. Indeed, to identify thehierarchical level of homology or homoplasy being specified, we shouldalways speak of ‘homologous as limbs, homologous as digits, homologousas a developmental process, homologous as a gene network, etc.,’ andditto for ‘homoplastic as . . . ’” (2003, 425). He is thus using “hierarchicallevel” to refer to both levels of hierarchical organization as well as levelsof generality within these hierarchical levels. By distinguishing between

8. For homology in the strictest sense, we will simply use the term “homology” or,after Owen (1843), “special homology.” Our “g-homology” should not be confusedwith Owen’s (1843) “general homology,” the latter being the homological relationshipbetween organisms and the archetype.


these two concepts, we are, as we will now argue, able to derive bothgeneral and serial homology from our account.

To better understand g-homology, consider the following example. Thethird cervical vertebra (C3) in one macaque is clearly homologous to C3in another macaque. This is what our account tells us, and this accordswith scientific practice. But suppose we ask the question whether the secondcervical vertebra (C2) in one macaque, O, is homologous to C3 in anothermacaque, O*. The answer that our account gives is that these vertebrae arenot homologous, although they are g-homologous. For there is completecontinuity of these traits on the phylogenetic pathway between the twomacaques but not complete correspondence—when moving from parent tooffspring along the phylogenetic pathway from O to O*, picking out thehomologous trait each step of the way (as our account instructs), one willpick out C2 each step of the way. On the other hand, when moving in thedirection from O* to O, one will pick out C3 each step of the way. Thus,T and T* will not be numerically identical each step of the way, so thereis not correspondence at the level of the traits in question. However, sup-posing that C2 and C3 are derived from a single feature at the next leveldown (the level of the developmental basis for the traits) either in O andO* themselves or in an organism ancestral to both O and O*, then ouraccount counts C2 in the first macaque and C3 in the second macaque asg-homologous. Whereas C3 in O and C3 in O* are homologous qua thirdcervical vertebrae, C2 in O and C3 in O* are homologous qua vertebrae.9

Although in this case C2 and C3 share the same developmental basisin all organisms from O to O*, this need not be the case. As the HDAHimplies, all that is needed is that C2 and C3 share a developmental basiseither in O and O* themselves or in an organism ancestral to O and O*.The developmental basis could therefore be quite distinct in O and O*.Thus, the semi-independence of homology at one level from homologyat other levels is mirrored by the semi-independence of the levels in g-

9. It is important to note that the parenthetical part of condition 2, which accountsfor g-homology, is not merely an ad hoc addition to the HDAH. The way in which itmodifies condition 2 to account for g-homology is precisely the way in which condition1 accounts for homology at distinct hierarchical levels: by appealing to the condition’sbeing met at L-1, although it is not met at L (the level of the traits in question). Tosee this, notice that just as condition 1 holds that T and T* can be homologous evenif there is not complete continuity at L (as long as there is continuity at L-1), so theparenthetical addition to condition 2 holds that T and T* can be g-homologous aslong as there is correspondence at L-1 (either in O and O* themselves or in an organismancestral to both O and O*), even if there is not complete correspondence at L. Sothis parenthetical part of condition 2 allows for g-homology in just the way in whichcondition 1 allows for homology at distinct hierarchical levels. We thus account forhomology and g-homology in a way that is as continuous as can be expected, giventhat g-homology is more general than homology.


homology. As we will now see, this has important implications for thenature of serial homology.

6.2. Serial Homology. As we have just seen, C2 in organism O andC3 in organism O* are not homologous but only g-homologous; it is C2in O and C2 in O* that are homologous, as are C3 in O and C3 in O*.But now consider the question of what the relationship is between C2and C3 within the same organism—traits that our account likewise labelsas g-homologous. As scientific practice has it, the relationship that theybear is one of serial homology. On our account, the serial homology oftwo traits, T and T*, is to be understood as a special case of their g-homology—the special case in which O and O* are numerically identical.In other words, in addition to T and T* being g-homologous between Oand a numerically distinct conspecific, O*, T and T* can bear the rela-tionship of g-homology within a single organism—and it is this case ofg-homology that we label “serial homology.”

There are two interesting and important implications of defining serialhomology in terms of g-homology. The first is that because g-homologyrequires only that T and T* have the same basis at L-1 (either in O andO* themselves or in an organism ancestral to both O and O*), preciselyhow ancestral the organism in which T and T* share a common basis atL-1 is can vary greatly: if T and T* are derived from the same featuresat L-1 in O (since in the case of serial homology, O and O* are identical,we refer here simply to O rather than to O and O*) or a recent commonancestor of O, then T and T* are serial homologues because of veryproximate causes. If, on the other hand, T and T* are derived from thesame features at L-1 but only in a very distant ancestor of O, T and T*are serial homologues because of very distant causes. It might be thoughtthat if the homology is based on a very distant ancestor, this is what ismeant by “deep homology.” But as we have articulated our position insection 5, deep homologies are a distinct phenomenon. We know of noterm for making this distinction and would suggest proximal serial hom-ologues for cases in which T and T* are derived from L-1 in O or a recentancestor of O and distal serial homologues for cases in which T and T*are derived from L-1 only in a distant ancestor of O. A parallel distinctionwill hold among the g-homologues that are not serial homologues: if theancestor in which the traits are derived from the same features at L-1 isa recent common ancestor of O and O* (in the case where O* is an ancestorof O, this recent common ancestor could just be O*), the traits will beproximal g-homologues, while if this ancestor is more distant they willbe distal g-homologues. Additionally, the HDAH correctly categorizesserial homologues that have no evolutionary history: the origin of a noveltrait T in O from a basis at L-1 shared by T* in O, T and T* will be


considered serial homologues because they are g-homologues found withina single organism.

The second important implication of defining serial homology as aspecial case of g-homology is that, given the connection between specialhomology and g-homology in our account, we successfully sidestep one ofthe major criticisms of the genealogical account—that under that accountthere is no continuity between serial and special homology. We will nowsuggest that, while the HDAH provides for continuity between serial andspecial homology, both the genealogical and developmental account fail todo so.

6.3. Serial Homology and the Shortcomings of Traditional Views. Wag-ner (1989) faults a strictly genealogical account of homology for implyingthat the concept of serial homology is at bottom a misnomer, since it isnot concerned with the relation between traits in ancestors and descen-dants: “This seems to imply that the similarity of two hairs on the sameanimal has a different cause than the similarity of two hairs from twomammalian species. . . . This is hard to believe” (54). As an example ofthis lack of continuity between serial and special homology, consider theaccount of serial homology proposed by Lauder (1994): “In my view,iterative (i.e., serial) homology simply refers to homology of one or moredevelopmental processes (or patterns of genetic covariation) at a greaterlevel of phylogenetic generality than the individual organism. To say thatcervical vertebra 4 is serially homologous to cervical vertebra 5 in anindividual mammal is simply to say that species in the Mammalia sharean homologous developmental pathway (or set of pathways) that producesserially arranged phenotypic structures similar in size and shape” (174).

First, there is no continuity between Lauder’s account of serial ho-mology and the genealogical account of homology. Whereas, on the ge-nealogical account, homology is based on the presence of the trait in acommon ancestor, Lauder’s view would have it that the ground of thehomology of cervical vertebrae 4 and 5 within a single organism is entirelydifferent: it is grounded in a fact of homology at the level of featureswithin species, not within individuals. More specifically, reference to serialhomology is nothing more than a shorthand for reference to the meresimilarity of size and shape between two traits within an organism, traitswhich are the product of a developmental process which is homologouswithin some higher-level taxon under which that organism falls. So wehave no continuity whatsoever between homology and serial homologyof traits on this view. Second, what account of homology at the level ofspecies is being employed here? It is difficult to see, on the face of it, howthe genealogical account of homology could be transferred seamlesslyfrom the case of organisms to the case of species. After all, whereas it is


clear whether two individual organisms share the relationship of ancestorand descendent, ancestor-descendent relationships become far less clearwhen we move to higher taxa, such as species. The genealogical account,in sum, is unable to provide for any continuity between special and serialhomology. What about the developmental account? Wagner (1989) arguesthat his developmental account, unlike the genealogical account, is ableto apply to serial homology and nonserial homology continuously. Foraccording to his account, “Structures from two individuals or from thesame individual are homologous if they share a set of developmentalconstraints, caused by locally acting self-regulatory mechanisms of organdifferentiation. These structures are thus developmentally individualizedparts of the phenotype” (62). On the face of it, it appears that the de-velopmental account achieves the desired continunity. But is it truly uni-fying? Recall that the developmental account presupposes a prior accountof the homology of developmental constraints. Given this, the develop-mental account can only be continuous between serial and nonserial ho-mology if the account of the homology of developmental constraintswhich it employs (but does not explicate) is continuous between serialand nonserial homology. Prior to an account of homology at the devel-opmental level, then, we must be agnostic about whether the develop-mental account is truly unifying. The HDAH, as opposed to the devel-opmental or genealogical accounts, does provide for continuity betweenspecial, serial, and general homology, without presupposing such conti-nuity at lower levels.

7. The Marriage of the Genealogical and Developmental Accounts. Forthe biologist reading this essay, two concerns are likely to emerge. First,what would adopting the HDAH account do to past homology determi-nations based on the genealogical or developmental accounts? (In otherwords, would the HDAH framework sufficiently remap the homology re-lation so that traits previously taken to be homologues should no longerbe considered as such?) And second, how is it possible to provide an accountof the homology relation without first providing an account of traits?

Although much of this essay has been spent pointing out the weaknessesof the developmental and genealogical accounts and pushing our alter-native, this alternative should not be seen so much as a replacement forthese accounts but more as a marriage of them: it is not that the gene-alogical and developmental accounts are wrong, in that they label thewrong set of traits as homologues. Rather, it is that they are incomplete—while they do a good job picking out homologues within a limited domain,they cannot pick them out in all domains. And this becomes especiallyclear when we consider homologies at multiple levels of generality, as wehave done in section 6.2. Our account combines important theoretical


insights from the genealogical and developmental accounts in a systematicway, so as to capture homologues across the restricted domains reachedby each of these mainstream accounts. Moreover, our account can be ofpractical use to biologists already accustomed to using either of thesemainstream accounts because, in thus systematizing their insights, it makesclear under what conditions each of them goes astray and under whatconditions each succeeds.

For the biologist, then, adopting the HDAH would not be a revolu-tionary act and would not undermine past work in fields like comparativeanatomy or evolutionary biology. The biological consensus that traits likefungiculture in attine ants is homologous across the Attini, or that thesecond and third cervical vertebrae in an individual macaque are serialhomologues, will not be undermined. Instead our account is simply point-ing out that the traditional accounts of homology, taken individually, donot have the theoretical resources to justify all such homology determi-nations. But the HDAH, by marrying the two accounts, is equipped witha set of resources for justifying these diverse homology determinations.

The advantages of the HDAH over the traditional accounts do not,however, extend to the question of how traits should be individuated. Aswas discussed in section 4, the HDAH account requires that traits at thedifferent levels be individuated independently of one another but does notprovide a framework for how this individuation should take place. Thisfact does not undermine the HDAH, since although homology deter-minations in practice require one to first individuate traits, theoreticalaccounts of homology show what kind of relation to one another traitsmust bear in order to be homologues, while leaving open the question ofwhat it is for something to be a trait. The questions what is a trait? andwhat is a homologue? can thus be addressed independently of one another,despite the fact that the biologist needs answers to both.

8. Conclusion. As one of the foundational concepts in the biological sci-ences, it is imperative that we work toward a clear and precise conceptof homology that is readily contrasted with related concepts such as thoseof homoplasy and deep homology. We are hopeful that the HDAH willhelp in this clarification. We have shown that the two main ways ofunderstanding homology—the genealogical and developmental ac-counts—fall short of being able to fully ground the concept of homologyand its relations to serial homology and what we call g-homology. Thealternative that we have provided draws on some of the concepts andstrategies of both of these accounts while avoiding the counterexamplesthat they generate. The HDAH draws on the strategy of the genealogicalaccount by requiring continuity along a phylogenetic pathway betweentwo organisms as a necessary condition for the homologousness of traits


had by those organisms, and on the strategy of the developmental accountby relaxing the constraint on what we mean by continuity—allowing alack of strict continuity at one level to be compensated for by continuityat the next level down. Through this hybrid account, biological samenessin the homological sense is given a new foundation, one that can groundbiological theory and practice and that is free of abstract archetypes.

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